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Decadal Environmental 'Memory' in a Reef Coral?

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Decadal Environmental 'Memory' in a Reef Coral? Brown BE, Dunne RP, Edwards AJ, Sweet MJ, Phongsuwan N. Decadal environmental 'memory' in a reef coral?. Marine Biology 2015, 162(2), 479- 483. Copyright: © Springer, 2015. The final publication is available at Springer via http://dx.doi.org/10.1007/s00227-014- 2596-2 DOI link to article: http://dx.doi.org/10.1007/s00227-014-2596-2 Date deposited: 17/02/2015 Embargo release date: 12 December 2015 This work is licensed under a Creative Commons Attribution-NonCommercial 3.0 Unported License Newcastle University ePrints - eprint.ncl.ac.uk Decadal environmental ‘memory’ in a reef coral? B.E. Brown 1,2 *, R.P. Dunne 3, A.J. Edwards 1, M.J. Sweet 4, N. Phongsuwan 5 1 School of Biology, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom 2 Environmental Research Institute, North Highland College, Castle Street, Thurso, Caithness KW14 7JD, United Kingdom 3 West Briscoe, Baldersdale, Barnard Castle DL12 9UP, United Kingdom 4 College of Life and Natural Sciences, University of Derby, Kedleston Road, Derby DE22 1GB, United Kingdom 5 Department of Marine and Coastal Resources, 120 Moo 3 Changwathana Road, Bangkok 10210, Thailand * Corresponding author e-mail: [email protected] Abstract West sides of the coral Coelastrea aspera, which had achieved thermo-tolerance after previous experience of high solar irradiance in the field, were rotated through 180o on a reef flat in Phuket, Thailand (7o50´N, 98o25.5´E) in 2000 in a manipulation experiment and secured in this position. In 2010 elevated sea temperatures caused extreme bleaching in these corals, however the former west sides of colonies (now facing east) retained 4 times higher symbiont densities than the east sides of control colonies which had not been rotated and which had been subject to a lower irradiance environment than west sides throughout their lifetime. The reduced bleaching susceptibility of the former west sides in 2010, compared to handling controls, suggests that the rotated corals had retained a ‘memory’ of their previous high irradiance history despite living under lower irradiance for 10y. Such long-term retention of an environmental ‘memory’ raises important questions about the acclimatisation potential of reef corals in a changing climate and the mechanisms by which it is achieved. Key words: environment, acclimatisation, memory, coral 1 Introduction Variability in bleaching patterns within individual coral colonies, subject to elevated temperatures, has been well documented in the field. Such patterns have been attributed to spatial distributions of resident symbiotic algal clades (Rowan et al 1997), localised high irradiance stress falling on upper coral surfaces (Fitt et al 1993) and experience– mediated physiological tolerances (Brown et al 2002a). In the latter example, western sides of the merulinid (Huang et al 2014) coral Coelastrea (formerly Goniastrea) aspera, which had received regular high solar irradiance, showed less bleaching and improved temperature tolerance compared with more shaded eastern sides during a major temperature-induced bleaching event in the Andaman Sea in 1995 (Brown et al 2000). C. aspera from inshore reef locations, where this phenomenon was observed, hosts only one Symbiodinium clade, namely D1a (Pettay and LaJeunesse 2009) and so bleaching patterns cannot be attributed to genetic differences in symbiotic algae as described in other studies (Rowan et al 1977). This superior temperature tolerance was attributed to higher levels of stress proteins and antioxidants in the coral host and improved xanthophyll cycling in Symbiodinium on western surfaces (Brown et al 2002a). The acquisition of thermal tolerance by western sides of C. aspera colonies led to striking bleaching patterns in the field in 1995, where eastern surfaces of many C. aspera colonies bleached stark white, while western sides were still highly pigmented. The majority of these colonies were estimated to be 4-6 years old and the time-scale of acquisition of thermal tolerance would therefore have been relatively short (2-3y) since colonies do not reach a size sufficient to receive differential solar irradiance regimes on east and west surfaces until they are at least 2y of age (Brown et al 1994). An earlier review (Brown and Cossins 2011) first raised the question of how long the irradiance ‘memory’, and the thermo-tolerance it conferred in these corals, might be retained in the absence of the environmental signal that first induced the tolerance. A manipulation experiment in 2000 where C. aspera colonies were rotated through 180o so that original west surfaces faced east and east surfaces faced west (McDougall et al 2006), together with an extreme bleaching event in 2010 (Brown and Phongsuwan 2012), provided an opportunity to assess the bleaching susceptibility of former western surfaces that had been orientated in a more shaded east-facing direction for 10y. Material and Methods Study Site and Coral Manipulation The study site is an intertidal reef flat at Ao Tan Khen on the SE tip of Phuket, Thailand (7o50´ N, 98o25.5´E) which has been a focus of study for over 35y and which has been described in detail in earlier work (reviewed in Brown et al 2011). In November 2000 a manipulation experiment was carried out on the inner reef flat which is dominated by the massive corals C. aspera and Porites lutea (McDougall et al 2006). C. aspera colonies (n=24), approximately 20cm mean diameter, were carefully detached from the reef using a hammer and stone chisel and rotated 180o before being cemented in their new position (hereafter termed ‘rotated’). An additional 24 colonies were detached from the reef and replaced in their original position to act as handling controls (hereafter termed ‘controls’) (Fig.1a). Earlier detailed levelling of the reef flat (Tudhope and Scoffin 1994) ensured that colonies were all placed at a similar height on the reef and 2 repeated observations through ebbing and flooding tides confirmed that both ‘rotated’ and ‘control’ colonies were exposed and covered by seawater at the same time. Figure 1 Location of ‘rotated’ and ‘control’ corals on the reef flat A) in November 2000 B) in May 2010 during the extreme bleaching event. 3 Environmental Data A long-term record of monthly mean sea temperatures for the region was obtained from the UK Metereological Office Hadley Centre (HadSST2). These values have been shown to reliably track ‘in situ’ thermistors at the site which have been in place for varying time periods since 1994 (Dunne 2012). Coral Sampling and Measurement of Symbiodinium Densities At the height of a severe bleaching event in June 2010 two hole punch samples (1.5cm diam) were collected from the east face of each of 5 colonies from ‘rotated’ and ‘control’ groups. One hole punch sample was used to estimate Symbiodinium density while the other was used for genetic analysis of the Symbiodinium clade diversity. Symbiodinium density was measured in fixed and decalcified coral samples using the standard methodology described in Brown et al (1999) while samples for algal genetic determination were preserved in molecular grade ethanol stored at -20 ̊ C and transported to the UK for analysis. Genetic Analysis of Symbiodinium DNA was extracted from all samples using Qiagen DNeasy Blood and Tissue kits. Variation in Symbiodinium was monitored using the ITS2 region, using the forward primer "ITSintfor2" and the highly conserved reverse primer that anneals to the LSU "ITS2CLAMP" (LaJeunesse et al. 2003). PCR mixture and protocol was the same as that described in Sweet (2013). Denaturizing Gradient Gel Electrophoresis (DGGE) was performed using the D-Code universal mutation detection system (Bio-Rad). PCR products were resolved on 10% (w/v) polyacrylamide gels containing a 30-60% denaturant gradient for 13 h at 60 °C and a constant voltage of 50 V. Gels were stained with 9 µl Sybr Gold (Sigma) in 50 µl of TAE for 20 min then washed in 500 ml 1X TAE for a further 30 min and visualized using a UV transilluminator. A subset of the dominant resulting bands were excised from DGGE gels, left overnight in Zigma Molecular grade H20, vacuum centrifuged, re-amplified with the ITS2 primers and sequenced using a Big Dye transformation sequence kit and sent to Genevision (Newcastle University, UK) for sequencing. Symbiodinium sequences were defined from DGGE band matching analysis using Bionumerics 3.5 (Applied Maths BVBA). Tolerance and optimisation for band-matching was set at 1%. Statistical Analysis The hypothesis to be tested was that Symbiodinium densities in ‘rotated’ colonies would be greater than in ‘control’ colonies. Data were normal and homoscedastic which would permit the use of the parametric one tailed t-test. However, to obtain a better estimate of the p value, a one-tailed exact permutation test (using the Package permTS; Fay and Shaw 2010) was run in R (R Core Team 2013). An analysis of similarity (ANOSIM) was conducted to test differences in the OUT patterns associated with Symbiodinium ITS gene assemblage. 4 Results and Discussion In May 2010 sea temperatures at the study site rose to unprecedented high levels (Figure 2) causing a major bleaching event during which all manipulated corals bleached (Figure 1b). Previous major coral bleaching events at the site were recorded only in 1991 and 1995 (Brown and Phongsuwan 2004) although higher temperatures were seen in other years (Figure 2). Annual photography of permanent photo-transects at the site showed only partial bleaching in C. aspera colonies on the reef flat in May 1991 and 1995 and 100% bleaching in May 2010 with no thermally-induced bleaching recorded in any other year (Brown unpubl.). Figure 2 Monthly mean sea temperatures (1946-2013) for the sea area around Phuket, Thailand from the HadSST 2 dataset. Years are highlighted when sea temperatures rose above 30.1oC. Symbiodinium densities in east sides of bleached ‘rotated’ colonies (i.e.
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